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Production of dissolved organic carbon and low-molecular weight organic acids in soil solution driven by recent tree photosynthate

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Abstract

Dissolved organic carbon (DOC) is an important component in the terrestrial carbon cycle. Yet, the relative importance of different inputs of DOC to the soil solution remains uncertain. Here, we used a large-scale forest girdling experiment to examine how the supply of recent photosynthate to tree roots and their mycorrhizal fungi affects DOC, in particular low-molecular weight organic acids (LMWOA). We also studied effects of tree girdling on non-structural carbohydrates in microorganism, and examined the effects of freezing of soil and the presence of roots in the soil samples on soil solution DOC and LMWOA in this experiment.

The concentration of DOC was reduced by 40%, while citrate was reduced by up to 90% in the soil solution by the girdling treatment. Other LMWOA such as oxalate, succinate, formate and propionate were unaffected by the girdling. We also found that girdling reduced the concentrations of trehalose (by 50%), a typical fungal sugar, and of monosaccharides (by 40%) in microorganisms in root-free soil. The effect of freezing on DOC concentrations was marked in samples from control plots, but insignificant in samples from girdled plots. Release of DOC from cell lysis after freezing was attributed equally to roots and to microorganisms.

Our observations suggest a direct link from tree photosynthesis through roots and their mycorrhizal fungi to soil solution chemistry. This direct link should impact solute transport and speciation, mineral weathering and C dynamics in the soil compartment. Importantly, our finding of a substantial photosynthate driven production of DOC challenges the paradigm that DOC is mainly the result of decomposition of organic matter.

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Abbreviations

DOC:

dissolved organic carbon

LMWOA:

low-molecular weight organic acids

EG:

early girdling

ECM:

ectomycorrhizal

References

  • Aitkenhead-Peterson JA, Kalbitz K (2005) Short-term response on the quantity and quality of rhizo-deposited carbon from Norway spruce exposed to low and high N inputs. J Pflanzenern Bodenk 186:687–693

    Article  Google Scholar 

  • Andersen CP, Nikolov I, Nikolova P, Matyssek R, Häberle K-H (2005) Estimating “autotrophic” belowground respiration in a spruce and beech forest:decreases following girdling. Eur J For Res 124:155–163

    Google Scholar 

  • Bhupinderpal-Singh., Nordgren A, Ottosson Löfvenius M, Högberg MN, Mellander PE, Högberg P (2003) Tree root and soil heterotrophic respiration as revealed by girdling of boreal Scots pine forest: extending observations beyond the first year. Plant Cell Environ 26:1287–1296

    Article  Google Scholar 

  • Cannell MGR, Dewar RC (1994) Carbon allocation in trees – a review of concepts for modelling. Adv Ecol Res 25:59–104

    Article  Google Scholar 

  • Christ M, David MB (1994) Fractionation of dissolved organic carbon in soil-water – effects of extraction and storage methods. Comm Soil Sci Plant Anal 25:19–20

    Article  Google Scholar 

  • Currie WS, Aber JD (1997) Modeling leaching as a decomposition process in humid montane forests. Ecology 78:1844–1860

    Article  Google Scholar 

  • Cromack K Jr., Sollins P, Graustein WC, Speidel K, Todd AW, Spycher G, Ching YL, Todd RL (1979) Calcium oxalate accumulation and soil weathering in mats of the hypogeous fungus Hysterangium crassum. Soil Biol Biochem 11:463–468

    Article  Google Scholar 

  • De Luca TH, Keeney DR, McCarty GW (1992) Effects of freeze-thaw events on mineralization of soil nitrogen. Biol Fert Soils 14:116–120

    Article  Google Scholar 

  • Ekblad A, Högberg P (2001) Natural abundance of C−13 in CO2 respired from forest soils reveals speed of link between tree photosynthesis and root respiration. Oecologia 127:305–308

    Article  Google Scholar 

  • Ekblad A, Boström B, Holm A, Comstedt D (2005) Forest soil respiration rate and delta C-13 is regulated by recent above ground weather conditions. Oecologia 143:136–142

    Article  Google Scholar 

  • Giesler R, Lundström U (1993) Soil solution chemistry-effects of bulking soil samples. Soil Sci Soc Am J 57:1283–1288

    Article  Google Scholar 

  • Giesler R, Lundström US, Grip H (1996) Comparision of soil solution chemistry assessment using zero-tension lysimeters or centrifugation. Eur J Soil Sci 47:395–405

    Article  Google Scholar 

  • Griffiths RP, Baham JE, Caldwell BA (1994) Soil solution chemistry of ectomycorrhizal mats in forest soil. Soil Biol Biochem 26:331–337

    Article  Google Scholar 

  • Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizospere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195

    Article  Google Scholar 

  • Hütsch BW, Augustin J, Merbach W (2002) Plant rhizodeposition-an important source for carbon turnover in soils. J Plant Nutr Soil Sci 165:397–407

    Article  Google Scholar 

  • Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Högberg MN, Nyberg G, Ottosson-Löfvenius M, Read DJ (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–792

    Article  Google Scholar 

  • Högberg MN, Högberg P (2002) Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil. New Phyt 154:791–795

    Article  Google Scholar 

  • Högberg P, Nordgren A, Ågren GI (2002) Carbon allocation between tree root growth and root respiration in boreal pine forest. Oecologia 132:579–581

    Article  Google Scholar 

  • Högberg MN (2006) Discrepancies between ergosterol and the phospholipid fatty acid 18:2 omega 6,9 as biomarkers for fungi boreal forest soils. Soil Biol Biochem 38:3431–3435

    Article  Google Scholar 

  • Jennings D (1995) The physiology of fungal nutrition. Cambridge Univ. Press, Cambridge UK, pp 377–397

    Google Scholar 

  • Jones DL (1998) Organic acids in the rhizosphere - a critical review. Plant Soil 205:25–44

    Article  Google Scholar 

  • Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phyt 163: 459–480

    Article  Google Scholar 

  • Kalbitz K, Solinger S, Park J-H, Michalzik B, Matzner E (2000) Controls on the dynamics of dissolved organic matter in soils: a review. Soil Sci 165:277–304

    Article  Google Scholar 

  • Kalbitz K, Schmerwitz J, Schwesig D, Mattzner E (2003) Biodegradation of soil-derived dissolved organic matter as related to its properties. 113:273–291

  • Kaiser K, Guggenberger G, Haumaier L, Zech W (2001) Seasonal variation in the chemical composition of dissolved organic matter in organic forest floor layer lechates of old-growth Scots pine (Pinus sylvestris L.) and European beech (Fagus sylvatica L.) stands in northeastern Bavaria, Germany. Biogeochemistry 55:103–143

    Article  Google Scholar 

  • Kusel K, Drake HL (1999) Microbial turnover of low molecular weight organic acids during leaf litter decomposition. Soil Biol Biochem 31:107–118

    Article  Google Scholar 

  • Lindahl B, Stenlid J, Finlay R (2001) Effects of resource availability on mycelial interactions and P-32 transfer between a saprotrophic and an ectomycorrhizal fungus in soil microcosms. FEMS Microb Ecol 38:43–52

    Article  Google Scholar 

  • Neff JC, Asner GP (2001) Dissolved organic carbon in terrestrial ecosystems: synthesis and a model. Ecosystems 4:27–48

    Article  Google Scholar 

  • Olsson P, Linder S, Giesler R, Högberg P (2005) Fertilization of boreal forest reduces both autotrophic and heterotrophic soil respiration. Global Change Biol 11:1745–1753

    Article  Google Scholar 

  • O’Leary W (1989) Practical handbook of microbiology. CRC Press, Florida USA

    Google Scholar 

  • Park J-H, Kalbitz K, Matzner E (2002) Resource control on the production of dissolved organic carbon and nitrogen in a deciduous forest floor. Soil Biol Biochem 34:813–822

    Article  Google Scholar 

  • Peterbauer T, Puschenreiter M, Richter A (1998) Metabolism of galactosylononitol in seeds of Vigna angularis. Plant Cell Phys 39:334–341

    Google Scholar 

  • Qualls RG, Haines BL, Swank WT, Tyler SW (2002) Retention of soluble organic nutrients by a forested ecosystem. Biogeochemistry 61:135–171

    Article  Google Scholar 

  • Reith F, Drake HL, Kusel K (2002) Anaerobic activities of bacteria and fungi in moderately acidic conifer and deciduous leaf litter. FEMS Microb Ecol 41:27–35

    Article  Google Scholar 

  • Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Ann Rev Plant Phys Plant Mol Biol 52:527–560

    Article  Google Scholar 

  • Schimel JP, Clein JS (1996) Microbial response to freeze-thaw cycles in tundra and taiga soils. Soil Biol Biochem 28:1061–1066

    Article  Google Scholar 

  • Scott-Denton LE, Rosenstiel TN, Monson RK (2006) Differential control by climate and substrate over the heterotrophic and rhizosperic components of soil respiration. Glob Change Biol 12:205–216

    Article  Google Scholar 

  • Smith WH (1979) Character and significance of forest tree root exudates. Ecology 57:324–331

    Article  Google Scholar 

  • Soil Survey Staff (1998) Keys to soil taxonomy. 8th edn. USDA-NRCS. Pocahontas Press, Blacksburg (VA), pp 338

  • Steinmann K, Siegwolf RTW, Saurer M, Körner C (2004) Carbon fluxes to the soil in a mature temperate forest assessed by13C isotope tracing. Oecologia 141:489–501

    Article  Google Scholar 

  • Strobel BW, Bernhoft I, Borggaard OK (1999) Low-molecular-weight aliphatic carboxylic acids in soil solutions under different vegetations determined by capillary zone electrophoresis. Plant Soil 212:115–121

    Article  Google Scholar 

  • Strobel BW (2001) Influence of vegetation on low-molecular-weight carboxylic acids in soil solution: a review. Geoderma 99:169–198

    Article  Google Scholar 

  • Subke J-A, Hahn V, Battipaglia G, Linder S, Buchman N, Cotrufo MF (2004) Feedback interactions between needle litter decomposition and rhizosphere activity. Oecologia 139:551–559

    Article  Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C Soil Biol Biochem 19:703–707

    Article  Google Scholar 

  • van Hees PAW, Lundström US, Giesler R (2000) Low molecular weight organic acids and their Al-complexes in soil solution-composition, distribution and seasonal variation in three podzolised soils. Geoderma 94:173–2000

    Article  Google Scholar 

  • van Hees PAW, Jones DL, Finlay R, Godbold DL, Lundström US (2005) The carbon we do not see––the impact of low molecular weight compounds on carbon dynamics and respiration in forest soils: a review. Soil Biol Biochem 37:1–13

    Article  Google Scholar 

  • Westergaard B, Hansen HCB, Borggaard OK (1998) Determination of anions in soil solutions by capillary zone electrophoresis. Analyst 123:721–724

    Article  Google Scholar 

Download references

Acknowledgements

We thank Katharina Steinman for valuable help in the field and Christina Kaiser for help with the carbohydrate analysis. The study received financial support from the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS; project 23.0161/98) to R.G. and from the Swedish Science Council (VR) and the EU (project FORCAST) to P.H.

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Authors and Affiliations

  1. Climate Impacts Research Centre, Department of Ecology and Environmental Science, Umeå University, Box 62, 981 07, Abisko, Sweden

    Reiner Giesler

  2. Department of Forest Ecology, Swedish University of Agricultural Sciences, 901 83, Umeå, Sweden

    Mona N. Högberg, Anders Nordgren & Peter Högberg

  3. Chemistry Department, The Royal Veterinary and Agricultural University, Thorvaldsensvej 40, 1871, Frederiksberg C, Denmark

    Bjarne W. Strobel

  4. Department of Chemical Ecology and Ecosystem Research, Chemical Physiology of Plants, University of Vienna, Althanstrasse 14, 1090, Vienna, Austria

    Andreas Richter

Authors
  1. Reiner Giesler
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  2. Mona N. Högberg
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  3. Bjarne W. Strobel
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  4. Andreas Richter
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  5. Anders Nordgren
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  6. Peter Högberg
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Correspondence to Reiner Giesler.

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Giesler, R., Högberg, M.N., Strobel, B.W. et al. Production of dissolved organic carbon and low-molecular weight organic acids in soil solution driven by recent tree photosynthate. Biogeochemistry 84, 1–12 (2007). https://doi.org/10.1007/s10533-007-9069-3

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  • DOI: https://doi.org/10.1007/s10533-007-9069-3

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